Misdirected attentional focus in functional tremor

Abstract

A characteristic and intriguing feature of functional neurological disorder is that symptoms typically manifest with attention and improve or disappear with distraction. Attentional phenomena are therefore likely to be important in functional neurological disorder, but exactly how this manifests is unknown. The aim of the study was to establish whether in functional tremor the attentional focus is misdirected, and whether this misdirection is detrimental to the movement, or rather reflects a beneficial compensatory strategy. Patients with a functional action tremor, between the ages of 21-75, were compared to two age and gender matched control groups: healthy control participants and patients with an organic action tremor. The groups included between 17 and 28 participants. First, we compared the natural attentional focus on different aspects of a reaching movement (target, ongoing visual feedback, proprioceptive-motor aspect). This revealed that the attentional focus in the functional tremor group, in contrast to both control groups, was directed to ongoing visual feedback from the movement. Next, we established that all groups were able to shift their attentional focus to different aspects of the reaching movement when instructed. Subsequently, the impact of attentional focus on the ongoing visual feedback on movement performance was evaluated under several conditions: the reaching movement was performed with direct, or indirect visual feedback, without any visual feedback, under three different instruction conditions (as accurately as possible/very slowly/very quickly) and finally as a preparatory movement that was supposedly of no importance. Low trajectory length and low movement duration were taken as measures of good motor performance. For all three groups, motor performance deteriorated with attention to indirect visual feedback, to accuracy and when instructed to move slowly. It improved without visual feedback and when instructed to move fast. Motor performance improved, in participants with functional tremor only, when the movement was performed as a preparatory movement without any apparent importance. In addition to providing experimental evidence for improvement with distraction, we found that the normal allocation of attention during aimed movement is altered in functional tremor. Attention is disproportionately directed towards the ongoing visual feedback from the moving hand. This altered attentional focus may be partly responsible for the tremor, since it also worsens motor performance in healthy control participants and patients with an organic action tremor. It may have its detrimental impact through interference with automatic movement processes, due to a maladaptive shift from lower- to higher-level motor control circuitry.

Keywords: attention; functional movement disorder; functional neurological disorder; treatment; visual feedback.

Figure 1

Natural attentional focus experimental setup. (A) Target jump: the target jumped to either side once when the cursor had passed one of five random thresholds between 19% and 69% of the direct trajectory. (B) Added deviation: an angular deviation to the left or the right of a fixed amplitude was added to the position of the cursor. The amplitude increased by 1º from trial to trial. The deviation was randomly added from one of five points between 19% and 44% of the direct trajectory onwards and persisted until the target was reached. (C) Experimental setup and screen display: after a countdown from three the target appeared at the top of the screen and the cursor was free to move from the starting position. When the target was reached it turned magenta [1,0,1]. Start and target dot: diameter 15 pixels (4.5 mm), colour white [1,1,1]. Cursor in A and B: 10 pixels (3 mm) [1,0,1]. For the target (D) and cursor (E) luminance changes, the cursor was initially white [1,1,1] and of the same size as the target (15 pixels). The luminance change occurred randomly at one of five points along 25 to 50% of the direct trajectory and reverted back to white [1,1,1] when a further 25% of the direct trajectory had been passed.

Figure 2

Typical trajectories and group durations. (A) For the direct versus indirect visual feedback conditions. (B) For the absent visual feedback versus baseline conditions. For each comparison, for which there was a statistically significant difference in path length, a typical trajectory for each condition is plotted, together with the group average durations. Note that 100 pixels correspond to 3 cm. The direct path between the start and target is 760 pixels, which corresponds to 22.8 cm. The change in tremulousness is difficult to appreciate in these small figures. Real size trajectories of the functional tremor group are provided in Supplementary Figs 1 and 2. For the durations, statistically significant differences are marked by asterisks: *P < 0.05, **P < 0.001. The box-and-whisker plots indicate the median, 25th and 75th percentile, upper and lower adjacent values and outliers.

Figure 3

Typical trajectories and group durations. (A) For the slow and fast versus baseline conditions, (B) the attention beyond the movement versus baseline conditions and (C) the movement to the start versus the baseline movement to the target conditions. For each comparison, for which there was a statistically significant difference in path length, a typical trajectory for each condition is plotted, together with the group average durations. Note that 100 pixels correspond to 3 cm. The direct path between the start and target in A is 760 pixels, in B and C it is 792 pixels. The change in tremulousness is difficult to appreciate in these small figures. Real size trajectories are provided in Supplementary Figs 3–5, 7 and 8. For the durations, statistically significant differences are marked by asterisks: *P < 0.05, **P < 0.001. The box-and-whisker plots indicate the median, 25th and 75th percentiles, upper and lower adjacent values and outliers. Supplementary Fig. 6 additionally shows typical trajectories for the beyond the movement and to the start conditions for the control groups for which there is no statistically significant difference in the path lengths between the two conditions.